J. Entomol. Res. Soc., 14(1): 95-105, 2012 ISSN:1302-0250

Seasonal Abundance of Horse (Diptera: Tabanidae) in Western Anatolia

Ferhat ALTUNSOY A. Yavuz KILIÇ

Anadolu University, Faculty of Science, Department of Biology, 26470, Eskişehir, e-mail: [email protected]

ABSTRACT Adult horse take blood meals from many including human, so they have known as serious pests wherever they occur and also are known vectors of numerous disease agents. Seasonal abundance of Tabanidae species was monitored during from May to September of 2005, 2006 and 2007 years, in Western Anatolia, Turkey. Totally, 7293 specimens from 52 species belonging to nine genera were collected and identified. Seasonal activities of ten most abundant species, Dasyrhamphis umbrinus, subcylindrica, aprica, Tabanus bifarius, Tabanus bromius, Tabanus lunatus, Tabanus portschinskii, Tabanus quatuornotatus, Tabanus rupium and Tabanus unifasciatus were analyzed. D. umbrinus, T. bifarius, T. quatuornotatus, T. unifasciatus reached their peak of abundance in June and others species reached their peak of abundance at July. The longest flight period from first week of May to mid-September was determined for the species Haematopota subcylindrica and Tabanus bromius. Moreover, Haematopota subcylindrica was the most abundant with 23.86% and followed by Tabanus bromius with 20.65%. The population peak of species, and also vector potential, for each year can be affected from climatic conditions. Nevertheless, results suggest that the time between from the mid-June to the third week of July can be considered as the potentially higher-risk period of mechanical transmission of pathogens by tabanids for the study area. Key words: Tabanidae, Seasonality, Flight Period, Western Anatolia, Turkey.

INTRODUCTION Tabanidae family has considerable significance in medical and veterinary entomology. Their importance is associated with both the transmission of diseases and the economic significance of stress resulting directly from bites, or indirect secondary infections such as anemia through blood loss, allergic responses, etc. (Chvala et al., 1972; Olsufjev 1977). Worldwide studies are subjected to this family due to the feeding behaviour of female tabanids (Cameron 1926; Mac Creary 1940; Blickle 1955; Bosler et al., 1974; Kniepert 1980; Andreeva 1989; Krcmar et al., 2005; Krcmar 2006; Andreeva et al. 2009; Altunsoy and Kılıç 2010). Numerous studies have investigated the seasonality of Tabanidae species in different regions of the world (Miller 1951; Strickman et al., 1986; Strickler et al., 1993; Mc Elligot and Lewis 1998; Krcmar 1999, 2005). Although the husbandry is so common in Turkey, the number of studies about distribution and seasonal activity of horse fly species are inadequate. 96 ALTUNSOY, F., KILIÇ, A. Y. Seasonal activity patterns of haematophagous could help to prevent disease transmission during population peaks of vector species, through proper control strategies. Therefore, improvement the knowledge on the field of seasonality and population dynamics of blood-sucking Tabanidae species will be resulted in the reduction of economic losses in meat and milk industry and quantify the risk of transmission of pathogens by these vectors (Krcmar 1999; 2005). Chvala et al., (1972) indicates that seasonal activity patterns of horse fly species depend on the geographical altitudes and seasonal conditions. Previous studies about seasonal abundance patterns in specify that the first species emerge in the second half of May and last in the middle of September (Chvala et al., 1972; Krcmar 1999, 2005). Furthermore, Krcmar (2005, 2006) was reported that populations of the economically important and human-attacking species reach their peak on the July and August. When all these data are evaluated, this study conducted in Turkey for the first time in the beginning of May and continued until the end of September, was repeated for a period of three years. The primary aim of the study was to monitor the seasonal activity of the horse fly species in the study area, and the secondary objective is the evaluation process of abiotic factors that affect seasonal activity on commonly observed species of Tabanidae family.

MATERIAL AND METHODS The study was performed in a swampy place, where is the centre of Quercus and Pinus forest, on the Yarımca Village that is 20 km away from the city centre of Eskişehir (39o 53’ 936” K, 30o 37’ 747” D). The field of study is chosen on the transition zone between two different climatic conditions; Mediterranean and terrestrial micro-climates. The study was started at the beginning of May and continued until the end of September, when the horse fly species were active, in years 2005, 2006 and 2007. Temperature values in study area ranged from -18oC in the winter to 35 oC in the summer, with a mean annual temperature of 7oC. Monthly climate data, including minimum, maximum and mean temperatures and relative humidity (RH) were also obtained for the whole study period from a hygrothermographs (Oregon Scientific OR-BAR208HGA) located on the Malaise traps regularly. Adult horse flies were collected with Malaise trap and water traps, on four days of each week (May to October of 2005, 2006-2007 years). Collections of adult samples were practiced at every 20 minutes through 08:00 to 19:00. The collected samples were killed in ethyl acetate-containing jars and transferred to the laboratory. Species identification was made based on the literature (Chvala et al., 1972; Olsufjev 1977; Yücel 1987; Schacht 1987; Leclercq 1966a, 1966b, 1967a, 1967b). Seasonal activities were analysed for the species represented by more than 1% of total collected specimens, which are Dasyrhamphis umbrinus, Haematopota 97 Seasonal Abundance of Horse Fly (Diptera: Tabanidae) in Western Anatolia subcylindrica, , Tabanus bifarius, Tabanus bromius, Tabanus lunatus, Tabanus portschinskii, Tabanus quatuornotatus, Tabanus rupium and Tabanus unifasciatus (Table 1). A nonparametric Kendall’s correlation coefficient test (SPSS 10.0 for Windows XP) was done to analyse the correlation between the seasonality of horse fly species and the corresponding abiotic factors (mean temperature and relative humidity).

RESULTS Totally, 7293 samples of 52 Tabanidae species belonging to nine genera were collected and identified over the 3 years study period. The statistical analyses showed that the relative humidity has negative significant effect (τ = -0.414 at p = 0.0008) while mean temperature have positive significant effect on the seasonal activity of horse fly species (τ = 0.33 at p = 0.008) (Figs. 1-15). Results of three-year study indicate that the Tabanus as the most abundant genus with 30 species. Haematopota genus with 8 species, Hybomitra, 4; Philipomyia, Dasyramphis and Chrysops 2 species for each; , Silvius and Therioplectes genus represented with 1 species, respectively (Table 1). Haematopota subcylindrica was the most abundant with 23.86 % followed by Tabanus bromius (20.65 %), Philipomyia aprica (14.57 %), Tabanus quatuornotatus (8.25 %), Tabanus bifarius (5.57 %), Dasyrhamphis umbrinus (4.80 %), Tabanus unifasciatus (4.75 %) Tabanus lunatus (3.65 %), Tabanus portschinskii (1.65 %) and Tabanus rupium (1.52 %). These ten species made up 89.27 % of the horse fly fauna on the study area. The flight activity occurrence of the most abundant two species T. bromius and H. subcylindrica were determined as non-corrupted for 3 years long, continuously. H. subcylindrica flight activity began in the first week of May and peaked on July in 2005 and 2007; but in 2006, the most intense flight activity observed on June. T. bromius also continued the flight activity from first week of May to last week of September during three years. However, population of this species peaked in July for each year (Table 1). On the other hand, activities of these species were not end at slowly raining days, which observed low-temperature and high-relative humidity.

The Research Results are Evaluated by Months 1. Species the most abundant on May are; D. umbrinus, H. subcylindrica, H. caucasi, H. caucasica, H. pilosa, P. aprica T. bromius, T. quatuornotatus and T. unifasciatus. The analyzes of 3 years study results make it clear that H.subcylindrica and T. quatuornotatus species are the most active horse fly species for May. 2. Species the most abundant on June are D. umbrinus, H. subcylindrica, P. aprica, T. bifarius, T. bromius, T. lunatus, T. quatuornotatus, T. rupium and T. unifasciatus. The species D. umbrinus T. bifarius T. quatuornotatus T. rupium and T. unifasciatus are determined as they peaked on June. Furthermore, T. rupium and T. unifasciatus have a peak in 2005 on July; P. aprica is the only one that has a peak in June 2007. 98 ALTUNSOY, F., KILIÇ, A. Y. 0 10 0 0 7 0 8 1 0 0 0 0 0 52 2007 5 0 0 0 0 0 0 5 8 5 6 0 0 16 2 0 204 5 8 11 15 117 116 257 484 June July August Sept. 2 143 376 0 15 May 0 0 0 0 2 0 0 0 0 0 0 0 4 0 0 2 0 0 6 53 15 2006 8 5 5 5 6 2 0 0 277 29 3 0 34 12 3 3 76 4 0 0 0 6 4 0 0 0 8 15 35 June July August Sept. 0 5 0 May 0 5 0 0 0 0 0 0 2 0 0 0 10 7 76 61 30 10 12 3 8 1 0 0 0 8 2005 8 13 0 0 0 16 22 0 0 7 26 0 0 0 9 30 25 8 204 22 686 68 5 15 18 157 138 513 85 June July August Sept. 00 32 44 12 29 0 0 0 0 4 0 0 0 7 3 0 0 0020 00000000100 0000 00000001 0 0300 01000002000 0020 00000000100 7 3 0 0 0 3000 0130000 0 0600 00600003000 0700 00400000000 0010 00010000100 0020 00010000100 0140 00000000100 0210 00000000100 0100 00200002000 0 0 6 0 0 0 0 0121 00020003 0 3 0 0 0 0010 00000000200 0010 00001000200 0 13 0 0 0 0 6 6 0 0 0 4 1 0010 00002000000 12 434 10 May Species abanus briani Leclercq Tabanus autumnalis L. Tabanus bifarius Loew Tabanus Tabanus armeniacus Kröber Tabanus Philipomyia zizaniae Leclercq Philipomyia aprica Meigen Hybomitra pilosa Loew Hybomitra ciureai Seguy Hybomitra caucasica Enderlein Hybomitra caucasi Szilady Haematopota subcylindrica Pandelle L. Olsufjev, Moucha & Chvala Haematopota scutellata Olsufjev, Haematopota ocelligera Kröber Haematopota longantennata Olsufjev Haematopota grandis Meigen Haematopota crassicornis Wahlberg Dasyrhamphis umbrinus Meigen Haematopota bigoti Gobert Dasyrhamphis carbonarius Meigen Silvius alpinus Scopoli Chrysops viduatus F. Chrysops caecutiens L. Tabanus exclusus Pandelle Tabanus Atylotus fulvus Meigen Tabanus eggeri Schiner Tabanus Tabanus cuculus Szilady Tabanus Tabanus cordiger Meigen Tabanus Tabanus bromius L. Tabanus T Table 1. Number of collected horse fly species. Table 99 Seasonal Abundance of Horse Fly (Diptera: Tabanidae) in Western Anatolia 3 2 0 10 5 8 3 0 0 0 5 15 2007 0 0 0 3 0 0 38 0 0 5 0 162 13 2 1421 132 27 5 11 87 25 68 June July August Sept. 45 1187 May 2 0 0 10 3 4 8 0 0 0 0 0 0 0 0 0 6 0 0 0 10 2 0 12 0 0 0 42 15 164 37 2006 8 8 11 25 18 27 335 96 0 0 0 6 18 334 June July August Sept. 8 0 0 35 May 3 3 33 3 0 0 0 0 0 1 0 0 0 6 4 0 0 0 14 2 0 0 2 2005 00 00300002000 11 35 25 1759 250 8 145 35 8 June July August Sept. 00000 0 000000100 2 0 00000000200 0 00033000200 00000000200 0 0 0 0 3 0 12 0 0 0 0410000700 00 08 20 0 32 385 3 9 8 10 00000000100 100002000 0 0 0 0 0 0 0 0 0 6 0 4 2 0 0 0 0 6 0 10 0 7 14 0 0 0 0 0 46 2 0 0 0 16 00200 0 00020000100 022300200060000000303 00000000010 00000000000 00010000 00000000020 00000000100 44 1490 May Species otal Tabanus glaucopis Meigen Tabanus golovi Olsufjev Tabanus indrae Hausser Tabanus laetetinctus Becker Tabanus leleani Austen Tabanus Tabanus lunatus F. Tabanus Therioplectes tricolor Zeller Tabanus maculicornis Zetterstedt Tabanus martini Kröber Tabanus miki Brauer Tabanus portschinskii Olsufjev Tabanus prometheus Szilady Tabanus quatuornotatus Meigen Tabanus Tabanus regularis Jaennicke Tabanus Tabanus rupium Brauer Tabanus Olsufjev, Moucha & Chvala spodopteroides Olsufjev, Tabanus spodopterus Meigen Tabanus Tabanus sudeticus Zeller Tabanus spectabilis Loew Tabanus tergestinus Egger Tabanus Andreeva terterjani Dolin & Tabanus tinctus Walker Tabanus unifasciatus Loew Tabanus T 1. (Contunied) Table 100 ALTUNSOY, F., KILIÇ, A. Y. 3. Species the most abundant on July are H. subcylindrica, P.aprica, T. bromius, T. lunatus and T. portschinskii. For each year, given species have a peak of population on July. However rare species; T. prometheus, T. spodopteroides and T. spectabilis are determined as they have a peak on July. 4. Species the most abundant on August are H. subcylindrica, P.aprica ve T. bromius. Furthermore, species those have a late activity behaviour T. glaucopis, T. terterjani and T. martini peaked on August. 5. Species the most abundant on September are H. subcylindrica, P.aprica, T. bromius and T. unifasciatus. Although the activity end is determined for H. subcylindrica and P. aprica on September 2007, T. lunatus is determined as active on September 2006.

DISCUSSION There is no effective method for control of horse fly species and prevent the economic losses in caused by tabanids. In some regions, attractant traps using for tried to reducing attacks of tabanids to the livestock and human (Lehane, 2005). However, the only effective method is to stay away from regions where the intense activity of horse fly species shows in. The identification of horse fly activity peaks is fundamentally important information required to develop control strategies and the pathogens it vectors. Different studies in the literature were conducted all over the world about seasonality of horsefly species, gonotrophic cycle and changes of flight activity of Tabanidae species by climatic factors (Roberts 1971; Barros 2001; Hribar et al., 2003; Krćmar 1999, 2005; Krćmar et al., 2002; Al-Talafha 2005). The studies of the seasonal abundance of horse fly are very important for the standpoint of medical and veterinary parasitology, because some species of tabanids participate in the transmission of agents of various diseases and cause economic losses in meat and milk industry (Chvala et al., 1972; Foil 1989; Vazzeille-Falcoz et al., 1997; Thomson and Connor, 2000). Generally are being attacked by tabanids during 4-5 month among a year. Adult female tabanids are obligated blood-suckers and in a need of blood-feeding before every hatching period (Auroi 1982; Krcmar et al., 2002). Perich et al., (1986) were reported that an average of 0.1 kg daily loss on bovine animal products, which was attacked by mean of 66 tabanids daily. A study on 500 cattle that are in use for animal husbandry at Lousiana clearly reports the daily yield loss of %1-2 percentage because the tabanid attacks (Foil et al., 1991; Leprince et al., 1992). This study presents the first featured report about seasonal activities of Tabanidae species for Turkey, which provides a large part of economic income from livestock sources. After a period of three years of study, seasonality of Tabanidae species spreading in the city of Eskişehir were observed and evaluated (Table 1). The similar results with previously studies, about seasonal abundance of horse fly species, were obtained in this study (Hribar et al., 2003; Krcmar 1999, 2005; Al-Talafha 2005). 101 Seasonal Abundance of Horse Fly (Diptera: Tabanidae) in Western Anatolia

Figs. 1-2. Flight activity; 1) in May of 2005, 2) in May of 2006.

Figs. 3-4. Flight activity; 3) in May of 2007, 4) in June of 2005.

Figs. 5-6. Flight activity: 5) in June of 2006, 6) in June of 2007.

Figs. 7-8. Flight activity; 7) in July of 2005, 8) in July of 2006. 102 ALTUNSOY, F., KILIÇ, A. Y.

Figs. 9-10. Flight activity; 9) in July of 2007, 10) in August of 2005.

Figs. 11-12. Flight activity; 11) in August of 2006, 12) in August of 2007.

Figs. 13-14. Flight activity; 13) in September of 2005, 14) in September of 2006.

Fig. 15. Flight activity in September of 2007. 103 Seasonal Abundance of Horse Fly (Diptera: Tabanidae) in Western Anatolia In the study area, tabanids were the most abundant during the summer season from the second half of May through the third week of September (Figs. 1-15). First emerged species were belonging to Hybomitra genus, which are H. caucasi and H. caucasica and later H. subcylindrica, T. unifasciatus and T. bromius and also last emerged species were T. sudeticus and T. martini. On the other hand, as previous studies have reported, it has been identified that the most intense activity and the maximum diversity of species occurs in July. The lowest activity and species diversity encountered in September. Populations of species H. subcylindrica, T. bromius and P. aprica, which are known as human attacking species, were peaked on July (Chvala et al., 1972; Krcmar, 2006). The results of this study have provided important information that can be used to develop more effective control strategies for horse flies not only in Turkey, but also neighbour countries. For example, the seasonal activity data from this study when linked livestock activities will help determine the most appropriate times for using control strategies for these important vectors. Seasonal abundance and activity vary depending on the diet and habitat preferences of species, and these variances affected by biotic and physical factors. However, evaluation of submitted results of this study and previous studies, significant difference in activity under different ecological conditions is observed for some species (Krcmar 1999, 2005). Especially, the wide spreading and the most intense two species in Europe; T. bromius and H. subcylindrica are reported as they show similar seasonal activity even under different ecological conditions In addition, these two species were collected even in rainy and low-temperature observed days. Based on the results of study, it can be clearly seen that some species are only active for certain months. The results indicate that Therioplectes tricolor, D. carbonarius, Haematopota ocelligera, Hybomitra pilosa, T. cordiger, T. leleani T. regularis are active on June, Haematopota crassicornis, H. longantennata, Hybomitra ciureai, T. cuculus, T. eggeri, T. laetetictus, T. prometheus, T. spodopteroides on July and T. terterjani on August only. Previous studies also reported the limited flight periods of these species (Chvala et al., 1972; Olsufjev 1977; Krcmar, 1999, 2005). Seasonal variation of average temperature and relative humidity vary from year to year. By implication of seasonal variance of abiotic factors, peak periods of populations and seasonal activity of Tabanidae species vary each year. As it can be seen in results, high values of rainfall and humidity, also low average temperature among the session in 2006 affected the collected individual numbers. It is reported by the comparison results that the degradation of collected samples in 2006, %74.7 according to 2005 year and %68.1 according to 2007 year (Table 1). We suggest that, seasonal activities of horse fly species also can be vary in different altitude or different places in Turkey. Consequently, we suggest that further studies should be conducted about geographic spreads and seasonal activities of species in different parts of Turkey. 104 ALTUNSOY, F., KILIÇ, A. Y. ACKNOWLEDGEMENTS This study is a part of a PhD thesis of Ferhat ALTUNSOY, submitted to Osmangazi University. I am grateful to Prof. Dr. Rimma Andreeva and Prof. Dr. Yalçın Şahin for their kind cooperation. This work was supported by the Research Foundation of Anadolu University (Project Number: 051043).

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Received: September 01, 2011 Accepted: February 06, 2012 106 ALTUNSOY, F., KILIÇ, A. Y.